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MYCOTAXON Volume LXXXIII, Pp MYCOTAXON Volume LXXXIII, pp. 19-57 July-September 2002 PHYLOGENY OF AGARICS: PARTIAL SYSTEMATICS SOLUTIONS FOR CORE OMPHALINOID GENERA IN THE AGARICALES (EUAGARlCS) Scott A. Redhead Systematic Mycology and Botany Eastern Cereal and Oilseed Research Centre Research Branch. Agriculture and Agri-food Ottawa. Ontario. Canada. KIA OC6 and Fran90is Lutzoni, Jean-Marc Moncalvo, and Rytas Vilgalys Department ofBiology. Duke University Durham. NC 27708-0338. USA Abstract: The taxonomy of species previously assigned to Ompha/ina sensu lato or Clitocybe is reevaluated in light ofrecent molecularly-based phylogenetic hypotheses. Nomenclatural complications involving generic and specific names, lectotypifications and changes to the Code are analysed. Lichenompha/ia gen. noy. (type Hygrophorus hudsonianus, syn. Ompha/ina hudsoniana) is proposed for Jichenized fonner omphalinas. Ampulloc/itocybe gen. noy. (type Agaricus c1avipes, syn. ClilOcyhe c1avipes) is erected for its type species. Arrhenia is emended to include greyish species fonnerly included in Omphalina, but excluding reddish brown species related to Ompha/ina pyxidata, the conserved lectotype for Omphalina. The genera Cantharellula, Chrysomphalina, Cerronema, Clabrocyphella, Gliophorus, Haasiella, Hygrophorus, Hygrocybe, Pseuduarmillariella, and Rickenella, and the generic names Botrydina, Coriscium, Leptoglossum, Phaeotellus, Phytocunis, and Semiomphalina are discussed. 20 Key words: basidiolichen, Ampulloclitocybe,Arrhenia, Lichenomphalia, Omphalina, Gerronema. Introduction As noted in the accompanying article on omphalinoid mushrooms that may have evolved outside ofthe Agaricales (Redhead et ai, 2002), the omphalinoid and clitocyboid habits represent simple agaric morphologies that presumably arose multiple times. This hypothesis is well-supported by analyses that distantly separate several omphalinoid clades, including a lineage encompassing Rickenella Raithelh., possibly outside ofthe Agaricales (Moncalvo et al. 2000 & 2002; Redhead et al. 2002). In the present paper, we discuss the systematics and biology of several genera with omphalinoid basidiomata, including clades containing the conserved lectotype for the name Omphalina Quel., viz. 0. pyxidata(Pers.: Fr.) Que!. (see Greuter et al. 2000, p. 192; see Kuyper 1995 for authorship), and type species for the names Arrhenia Fr., Leptoglossum P. Karst., and Phaeotellus Kuhner & Lamoure, as well as the lichenized omphalinoid taxa previously referred to a lichenized genus for which the rejected names Phytoconis Bory, Botrydina Breb., and Coriscium Vain. (see Greuter et al. 2000, pgs. 393-395), were applied. The discussion necessarily involves the generic name Gerronema Singer (1951 a), because Singer (1970, 1986), and those who followed his classification, included the lichenized omphalinoid taxa within the enlarged concept he ultimately adopted for that genus. Stereotypical omphalinoid species fall into at least five inferred lineages within the greater Agaricales (= euagaric clade) using ITS and LSU data (Lutzoni 1997) and as supported by LSU data alone but using a much larger taxon sampling (Moncalvo et al. 2000 & 2002). These lineages are: (1) Gerronema sensu stricto (Singer 1951 a, emended by Redhead 1986) non Singer (1986), e.g., G. strombodes (Berk. & Mont.) Singer and G. subclavatum (Peck) Singer ex Redhead; (2) Chrysomphalina ClemenlYon sensu stricto (emended by Redhead 1986, Norvell et al. 1994) non Clemen~on (1982), e.g., C. chrysophylla (Fr.) ClemenlYon and C. grossula (Pers.) Norvell et al. (syn. Omphalina wynniae (Berk. & Br.) Ito); (3) the primarily bryophilous grey and brownish grey 2\ pigmented Arrhenia-Phaeo/ellus-Omphalina epichysium clade; (4) the lichenized omphalinas (Botrydina & Phytoconis of Redhead & Kuyper 1987, 1988, Norvell et al. 1994, Kuyper 1995); and (5) the Omphalina pyxidata group =Clitocybe sect. Pyxidatae sensu Bigelow (1974, 1985) and Lamoure (1974) pro par/e. A distinct omphalinoid lineage, (6) e.g., Rickenella and allies (Can/harellopsis Kuyper, Corylidia P. Karst., Loreleia Redhead et aI., Contumyces Redhead et aI., Sphagnomphalia Redhead et al.), which possibly evolved independently outside of the Agaricales (Moncalvo et a!. 2000 & 2002), is treated in a separate paper (Redhead et a!. 2002). All 6 lineages were previously supported by the equally weighted parsimony and maximum likelihood analyses ofthe combined ITS and LSU data set (Lutzoni 1997, figs. 5a, 7). In larger taxon samplings (Moncalvo et al. 2000 & 2002), these clades of omphalinoid agarics often appear separated from each other and interspersed with clades of agarics and other fungi not previously analysed by Lutzoni (1997), some being additional omphalinoid agarics. We reproduce Lutzoni's (1997, fig. 7) as our Fig. 1, but with the various clades reclassified and renamed as discussed below. Taxonomy and nomenclature Gerronema was originally proposed for lignicolous tropical species (S inger 195 Ia) that were latter characterized, in part, by the presence of sarcodimitic tissues (Redhead 1986, Norvell et a!. 1994). Two such species, G. strombode.'l and G. .'lubclava/um, formed a monophyletic unit in the analyses by Lutzoni (1997). Subsequently they were shown to be distantly related to other omphalinas (Moncalvo et a!. 2000). In a much larger analysis (Moncalvo et al. 2002), these two species ofGerronema cluster with other taxa with sarcodimitic tissues (e.g., with species assigned to Clitocybula (Singer) Metrod, Hydropu.'l (KUhner) Singer, Megacollybia Kot!. & Pouz., cf. Redhead, 1987), which together form a well-supported lineage (to be treated in a separate paper). Hence, neither the lichenized omphalinas nor Rickenella and alljes are closely related to Gerronema sensu stricto. 22 1III••I1!1!1•••: Gertooema SlJtdava'u~' ] Gerronema 100 Gstrombcdes 'Hygxcybe' cilrinopallida ] "Hygrocybe' ~!I!!!!I.--~ g!"Jss~Ja • Chrysomp/lalina ] Chrysompha/ina cnryscpr.,1la Agaricaies ClJr;SWo:;i!iili11a A veiutlpeS A. epc.~ysium A sphagnicol. A. ~or.Olis _-- A. chlorocyanea Arrhenia Alobaia A awiscalpium 79 A. obs~urata A. griseopalljda 52 JIII.IIII!••• L. ve/urina 100 .c=7:L gnS€Ra L---""-----L.a1pma Uchenomphalia """'F,i:O---- L lJu·jscmana ----L. umbellifera op}'Xida!a ] o ,'i~ulicola Omphalina "CIilocyre'laterilia Spn,,;nompllaJia bre'libasidiata ....--------- LOIe;e.'c mc'C~;;n'iae RJckenella meilea hymenochaetoid clade 93 Rpse-JJOg'iseila ---- C:lI~umyces rosena MuftidiMJla coryJlC..idEs I(~M-:. .···········11!1100"v vema!is 1nucleotide substitution/100 s~es Fig. 1. Most likely phylogenetic tree for Omphalinoid mushrooms based on a combined nuclear LSU and ITS rONA data set. Adapted from Lutzoni (1997, Fig. 7). Note the revised labelling ofthe clades proposed here and that "wynniae" and "grossula" are combined as C. grassula. 23 "Chrysomphalina" nom. invalid. (Haas,1962) was coined for two carotenoid forming taxa. The "type" C. chrysophylla, was retained in Chrysomphalina CI<~men90n ( 1982) when the name was validated, while the other, flaasiella venustissima (Fr.) Kot!. & Pouz.. was excluded and treated in the genus Haasiella Kotlaba & Pouzar (1966): see also Kost (1986) and Chiaffi & Surault (1996). Neither of the two presently recognized Haasiella species have been sequenced, but it seems possible that Chrysomphalina species might be their closest allies, and if nested among them. the name Haasiella would have priority. Following a detailed anatomical study, Kost (1986) however, concluded they were not closely allied. When Chrysomphalina was val idated by Clemen~on (1982), he included two species. the type. C. chrysophylla, and Gerronema strombodes. while excluding ll. venustissima. As indicated above, G. stromhodes is unrelated to C. chrysophylla. Additionally, the European concept of"G. strombodes" represented a misapplication of that name. Gerronema strombodes is restricted to eastern North America. The European taxon known to Clemen<yon as "G. strombodes" represents a different species, G. xanthophyllum (Bres.) Norvell et al.. also a true Gerronema (Norvell et al. 1994; Birrer 2000). As characterized by Norvell et al. (1994), Chrysomphalina accommodates lignicolous, c1ampless, carotenoid forming, omphalinoid taxa with nonamyloid thin-walled spores. pachypodial subhymenia, and monomitic tissues. Chrysomphalina, as thus defined, appears to be a monophyletic taxon allied firstly to a sister genus Hygrophorus Fr. (Moncalvo et al. 2000 & 2002), and possibly allied to other hygrophoroid genera (Lutzoni 1997; Moncalvo et al. 2000 & 2002). The genus Hygrophorus sensu stricto (e.g., H. bakerensis A.H. Smith & Hesler, H. sordidus Peck) is clearly a distinct lineage and genus, distinguished by a presumed obligate ectomycorrhizal symbiosis, absence of carotenoids (pigmented by sundry other pigments, Gill & Steglich 1987). possession ofa different chemistry, and clamp connection formation. Chrysomphalina species have elongated basidia (Norvell et al. 1994) and because of the pachypodial subhymenium, a somewhat divergent lamellar trama, perhaps homologous to the divergent, slightly differently arranged lamellar tramas characterizing Hygrophorus sensu stricto. 24 The combined phylogenetic analyses by Lutzoni (1997) sometimes placed HJlgrocybe citrinopallida (A.H. Smith & Hesler) Kobayasi (another hygrophoroid taxon) in proximity to Chrysomphalina (with weak support). The analyses by Moncalvo et al. (2000, fig. 2, clade "K") sometimes shifted it closer (also with weak support) to the lichenized omphalinas ("phytoconis") and Arrhenia
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